SIP-enabled multi-omics reveals soil microbiome responses to drought and rehydration

Abstract

The activity of the soil microbiome, and its balance of anabolic (organic C consuming) and catabolic (CO2-releasing) reactions, determines the magnitude and direction of soil carbon fluxes. Over half a century of research has revealed that soil water dynamics are key controllers of microbial activity. With increasing hydroclimate volatility expected across many regions of the Earth, there is a greater need to describe and quantify microbial responses to drought and rehydration cycles. In this study, we conducted rainfall exclusion experiments at two archetypical Mediterranean-type field sites. After rainfall exclusion and subsequent soil rehydration, we applied a SIP-enabled, multi-omics methodology to generate a multi-faceted case study of microbial growth, greenhouse gas fluxes, and the forms of carbon that drive both. Our results indicate that rehydration increases microbial anabolic processes by orders of magnitude, shifting cell generation times from years to days within just minutes. High-intensity drought increases the lag period before microbial growth resumes, but both stable-isotope probing and metagenomic inference agree that microbial communities exhibit greater capacity for rapid growth following drought stress. Furthermore, significant shifts in the soil metabolome are observed following drought and rehydration, implicating specific osmolytes as key to the microbial response and indicating metabolite diversity as a key modulator of microbiome functioning. Together, our results provide constraints on microbial activity rates in soil and mechanisms underpinning microbial responses to drought and rewetting. These findings motivate further research into microbial responses under increasingly volatile hydroclimate regimes and downstream contributions to the global carbon cycle. Significance StatementSoil is a major global store and source of carbon. The microbiome determine the fate of soil organic carbon, and the microbiome is ultimately controlled by soil water dynamics. Early, innovative experiments by H.F. Birch defined "The Birch Effect" - the observation that soils emit CO2 following drying and subsequent rehydration. However, it remains unclear when, and to what magnitude, soil microorganisms are actively growing following this rehydration, and what biological mechanisms explain the observed CO2 pulse. In this work, we apply an array of methodologies to address this question, describing rates of microbial growth during drought and rewetting. Our results provide crucial insights into how soil microbiomes will respond to increasing hydroclimate volatility across the globe.